ABSTRACT

We report metagenomic sequencing analyses of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) RNA in composite wastewater influent from 10 regions in Ontario, Canada, during the transition between Delta and Omicron variants of concern. The Delta and Omicron BA.1/BA.1.1 and BA.2-defining mutations occurring in various frequencies were reported in the consensus and subconsensus sequences of the composite samples.

ANNOUNCEMENT

The emergence and global spread of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) (genus Betacoronavirus, family Coronaviridae) variants of concern (VOCs) pose a significant threat to global health (1, 2). SARS-CoV-2 is shed in human fecal matter and less so in urine by infected individuals, and its detection in wastewater triggered global interest in tracking the dissemination of its VOCs (3, 4). The province of Ontario and other jurisdictions have adopted genomic surveillance of wastewater for monitoring known and emerging SARS-CoV-2 VOCs in the community (512).
We collected 24-h composite samples of raw influent from 28 wastewater treatment plants in 10 regions across Ontario between November 2021 and February 2022 (n = 48) (Table 1) as part of the COVID-19 Regional Genomic Initiative (CORGI) in Ontario. Nanotrap magnetic virus particles (Ceres Nanosciences) were added to 50-mL wastewater samples to capture and concentrate the virus, followed by RNA extraction with the QIAamp viral RNA minikit (Qiagen) according to the manufacturer’s instructions. The CDC N1 and N2 regions were detected in the RNA samples with one-step reverse transcriptase quantitative PCR (RT-qPCR) performed on QuantStudio 5 (Thermo Fisher Scientific) (13) by using the 2019-nCoV CDC RUO kit (IDT, Coralville, USA) and TaqPath master mix (Thermo Fisher Scientific) as described (14). Wastewater samples with a cycle threshold of ≤35 were sequenced. For genomic sequencing, cDNA synthesis was performed using the SuperScript IV first-strand synthesis system (Thermo Fisher Scientific). SARS-CoV-2 amplicons were generated as previously described (15) but with ARTIC V4 primers (https://github.com/artic-network/artic-ncov2019/tree/master/primer_schemes/nCoV-2019). DNA libraries were generated using the Nextera XT DNA library prep kit (Illumina). Paired-end (2 × 150 bp) sequencing was performed using the MiniSeq system (Illumina). Raw sequence reads were analyzed using ViralRecon v2.4.1 (16). Variants were called with iVar v1.3.1 (17) using minimum quality and depth of 15 and 10, respectively. Consensus and subconsensus sequences were defined using mutation frequency thresholds of >50% and 10 to 50%, respectively. Variant lineages were inferred using Pangolin v3.1.20 (18). Default parameters were used for all tools unless otherwise specified.
TABLE 1
TABLE 1 Summary of sequencing data of the samples
Sample IDDate of collection (day-mo-yr)aSampling pointWastewater sample location IDRegionGPS coordinatesNo. of input reads% mapped reads% breadth of coverageVariant detected (consensus)Variant detected (subconsensus)SRA accession no.
109_229-Nov-21Frontenac WWTP-1Kingston/Ravensview WWTPFrontenac44.241251, −76.4206163,859,51080.3999.08Delta sublineage AY.25NoneSRR18762211
1712-Dec-21Durham WWTP-1Midland/S3.2.12.21Durham44.75695003, −79.874838452,990,08055.6596.74Delta sublineage AY.25.3NoneSRR18680489
1153-Dec-21Windsor WWTP-1Windsor Lou Romano WRP 172Windsor42.28384, −83.085272,728,91058.4998.18Delta B.1.617.2NoneSRR18680486
1173-Dec-21Windsor WWTP-2Leamington PCC 148Windsor42.03443, −82.588502,794,61443.3298.17Delta sublineage AY.103NoneSRR18680474
1705-Dec-21Durham WWTP-2Ajax/F07.5.12.21Durham43.83831355, −79.04184192,828,28690.1696.66Delta sublineage AY.121Traces of Omicron BA.1SRR18680490
1745-Dec-21Durham WWTP-3Orillia/S4.5.12.21Durham44.59004157, −79.41322972,917,70896.1996.47Delta sublineage AY.25.3NoneSRR18680488
1166-Dec-21Windsor WWTP-1Windsor Lou Romano WRP 173Windsor42.28384, −83.085272,649,64054.0590.05Delta sublineage AY.4NoneSRR18680485
1186-Dec-21Windsor WWTP-2Leamington PCC 149Windsor42.03443, −82.588503,013,59444.3997.40Delta sublineage AY.103NoneSRR18680463
1508-Dec-21Northern Ontario WWTP-1Sudbury/TPKL221208Northern Ontario46.4655660272402, −81.03285571662952,145,83030.5798.75Delta sublineage AY.74NoneSRR18680452
1559-Dec-21Toronto WWTP-1-Site 1S2A-177Toronto43.73584, −79.4958322,767,23652.6696.52Delta B.1.617.2Traces of Omicron BA.1SRR18680491
17613-Dec-21Windsor WWTP-2Leamington PCC 152Windsor42.03443, −82.588502,837,33896.1497.52Delta sublineage AY.103NoneSRR18680487
28415-Dec-21Halton WWTP-1Maplehurst Correctional ComplexHalton43.520000, −79.9000003,446,19499.6499.14Delta sublineage AY.25.1NoneSRR18680462
21017-Dec-21Guelph WWTP-1GuelphWellington43.520000, −80.2700002,458,38075.0296.74Delta sublineage AY.39Omicron BA.1SRR18680480
20820-Dec-21Guelph WWTP-1GuelphWellington43.520000, −80.2700003,406,43667.0598.86Omicron BA.1Delta B.1.617.2SRR18680481
19121-Dec-21Frontenac WWTP-2Loyalist/Amherstview WPCPFrontenac44.233127, −76.6609883,231,11449.1398.79Omicron BA.1Delta B.1.617.2SRR18680484
20021-Dec-21Niagara WWTP-1Crystal Beach Wastewater Treatment Plant (Fort Erie)Niagara42.860000, −79.0600003,075,43635.1099.69Omicron BA.1.1Delta B.1.617.2SRR18680482
21122-Dec-21Guelph WWTP-1GuelphWellington43.520000, −80.2700003,053,44680.9998.71Omicron BA.1.1Delta B.1.617.2SRR18680479
19223-Dec-21Frontenac WWTP-3Eastern Ontario/HawkesburyFrontenac45.611676, −74.5960914,867,03096.3998.12Omicron BA.1.1Delta B.1.617.2SRR18680483
28729-Dec-21Halton WWTP-1Maplehurst Correctional ComplexHalton43.520000, −79.9000003,058,08891.5199.08Delta sublineage AY.25.1Traces of Omicron BA.1SRR18680461
2503-Jan-22Frontenac WWTP-4Kingston/Cataraqui Bay WWTPFrontenac44.214819, −76.5507223,616,51882.8998.34Omicron BA.1.1Delta B.1.617.2, Traces of Omicron BA.2SRR18680467
3043-Jan-22Niagara WWTP-2Queenston Wastewater Treatment PlantNiagara43.160000, −79.0500003,891,57476.6898.88Omicron BA.1.1Delta B.1.617.2SRR18680460
2224-Jan-22Durham WWTP-4Courtice WWTP/C04.4.1.22Durham43.87131928, −78.75597783,276,02668.0598.29Omicron BA.1.1Delta B.1.617.2SRR18680478
2275-Jan-22Toronto WWTP-1-Site 2S2B-167Toronto43.76187, −79.5083883,884,77298.5597.02Omicron BA.1.1NoneSRR18680477
2295-Jan-22Toronto WWTP-1-Site 3S1B-190Toronto43.730131, −79.5495783,068,43673.8797.54Omicron BA.1.1NoneSRR18680476
2515-Jan-22Frontenac WWTP-5Eastern Ontario/Hawkesbury WWTPFrontenac45.611676, −74.5960913,373,87867.6998.40Omicron BA.1Delta B.1.617.2SRR18680466
2306-Jan-22Waterloo WWTP-1Waterloo 845R-I-B 1/6Waterloo43.48509, −80.504122,655,47297.8499.68Omicron BA.1.1Delta B.1.617.2SRR18680475
2316-Jan-22Waterloo WWTP-2Galt 847R-I-B 1/6Waterloo43.340827, −80.3133573,138,93498.7599.59Omicron BA.1.1Delta B.1.617.2SRR18680473
2326-Jan-22Waterloo WWTP-3Kitchener 846R-I-B 1/6Waterloo43.396587, −80.4210803,486,77888.3699.71Omicron BA.1.1Delta B.1.617.2SRR18680472
2337-Jan-22Waterloo WWTP-4Peel 830F-I-B 1/7Waterloo43.7546220, −79.62640072,987,08653.2999.57Omicron BA.1.1Delta B.1.617.2SRR18680471
2357-Jan-22Waterloo WWTP-5York 831F-I-B 1/7Waterloo43.8456555, −79.33503152,720,06076.9698.40Omicron BA.1.1NoneSRR18680470
25410-Jan-22Northern Ontario WWTP-1Sudbury/TPKL220110Northern Ontario46.4655660272402, −81.03285571662953,003,88015.2799.69Omicron BA.1.1Delta B.1.617.2SRR18680465
30710-Jan-22Guelph WWTP-1GuelphWellington43.520000, −80.2700003,532,70299.7597.55Omicron BA.1.1Delta B.1.617.2SRR18680459
24511-Jan-22Toronto WWTP-1-Site 1S2A-187Toronto43.73584, −79.4958322,095,67698.7399.77Omicron BA.1.1Delta B.1.617.2SRR18680469
36812-Jan-22Niagara WWTP-3Port Weller Sewer Treatment PlantNiagara43.230000, −79.2200003,412,74294.39100.00Omicron BA.1.1Delta B.1.617.2SRR18680450
24813-Jan-22Toronto WWTP-1-Site 1S2A-189Toronto43.73584, −79.4958323,149,96891.6998.63Omicron BA.1.1Delta B.1.617.2SRR18680468
36513-Jan-22Niagara WWTP-4Baker Road Wastewater Treatment Plant (Grimsby)Niagara43.190000, −79.5400002,374,70698.3699.00Omicron BA.1.1Delta B.1.617.2SRR18680451
33014-Jan-22Halton WWTP-1Maplehurst Correctional ComplexHalton43.520000, −79.9000003,637,03097.0299.69Omicron BA.1.1Delta B.1.617.2SRR18680458
34114-Jan-22Guelph WWTP-1GuelphWellington43.520000, −80.2700003,529,34674.8597.64Omicron BA.1.1Delta B.1.617.2SRR18680454
25717-Jan-22Northern Ontario WWTP-1Sudbury/TPKL220117Northern Ontario46.4655660272402, −81.03285571662953,175,68691.7799.70Omicron BA.1.1Delta B.1.617.2SRR18680464
37317-Jan-22Northern Ontario WWTP-2Sault Ste. Marie/TPSSM220117Northern Ontario46.5057224005555, −84.257395000293,313,90489.7799.00Omicron BA.1.1Delta B.1.617.2, Omicron BA.2SRR18680448
33818-Jan-22Niagara WWTP-5Niagara Falls-Stamford Wastewater Treatment PlantNiagara43.120000, −79.0900002,917,97296.8399.71Omicron BA.1.1Delta B.1.617.2SRR18680455
35918-Jan-22Durham WWTP-5Corbett WWTP/OUT/A02.18.1.22Durham43.85542682, −78.892483012,366,05485.0299.00Omicron BA.1.1Delta B.1.617.2SRR18680453
33219-Jan-22Halton WWTP-1Maplehurst Correctional ComplexHalton43.520000, −79.9000003,260,30240.8899.66Omicron BA.1.1Delta B.1.617.2SRR18680457
33321-Jan-22Halton WWTP-1Maplehurst Correctional ComplexHalton43.520000, −79.9000003,834,21099.5399.21Omicron BA.1.1Delta B.1.617.2SRR18680456
37226-Jan-22Northern Ontario WWTP-1Sudbury/TPKL220126Northern Ontario46.4655660272402, −81.03285571662952,985,94899.15100.00Omicron BA.1.1Delta B.1.617.2SRR18680449
4215-Feb-22Ottawa WWTP-1Ottawa influentOttawa45.461111, −75.5891672,634,06293.9996.00Omicron BA.1.1NoneSRR18680447
4227-Feb-22Ottawa WWTP-1Ottawa influentOttawa45.461111, −75.5891672,482,60899.9596.00Omicron BA.1.1NoneSRR18680446
4239-Feb-22Ottawa WWTP-1Ottawa influentOttawa45.461111, −75.5891672,668,09850.4795.00Omicron BA.1.1NoneSRR18680492
a
Data in the table are sorted by date of collection. WWTP, wastewater treatment plant.
We received 148,603,298 total reads across all 48 samples (mean, 3,095,902; range, 2,095,676 to 4,867,030). In most of the samples (85%; n = 41), ≥50% of reads mapped to the SARS-CoV-2 Wuhan strain. The average breadth of coverage of the consensus sequences generated was 98%. In consensus sequences, the Delta variants, including 8 sublineages, were detected in 14 samples from 7 regions in December 2021 (Table 1). Omicron BA.1/BA.1.1 was detected in 34 samples collected from all the regions studied except in Windsor, located in the extreme southwest of the province (Fig. 1). In subconsensus sequences, 26 samples contained the Delta VOC, 2 samples contained both Delta and Omicron BA.2 mutations, while traces (≤6 mutations) of Omicron BA.1-defining mutations were detected in 4 samples. Overall, multiple SARS-CoV-2 VOCs were detected in 32 samples (Table 1). Collectively, continuous genomic surveillance of wastewater provides sufficient specificity to infer individual VOC lineages in mixed samples and is effective for monitoring SARS-CoV-2 VOCs in the community.
FIG 1
FIG 1 Heatmap showing estimated frequencies of Omicron (BA.1) mutations in composite samples of wastewater influent from 10 regions across Ontario. Each column represents a sample, and they are ordered by date of collection. Each row represents the genomic locus of a BA.1-defining mutation (https://github.com/cov-lineages/constellations/tree/main/constellations/definitions). Colors depict the percentage frequency of mutations in the samples; the deeper the color, the higher the mutation frequency. The heatmap was generated using VCFparser v1.0.0 (https://github.com/kbessonov1984/VCFParser).

Data availability.

The metagenomic sequences are available in the NCBI Sequence Read Archive under BioProject accession number PRJNA824537.

ACKNOWLEDGMENT

This project was funded by Ontario Genomics through the COVID-19 Regional Genomic Initiative (CORGI), Ontario.

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Information & Contributors

Information

Published In

cover image Microbiology Resource Announcements
Microbiology Resource Announcements
Volume 11Number 721 July 2022
eLocator: e00362-22
Editor: Simon Roux, DOE Joint Genome Institute
PubMed: 35638829

History

Received: 15 April 2022
Accepted: 9 May 2022
Published online: 31 May 2022

Contributors

Authors

Canadian Research Institute for Food Safety, Department of Food Science, University of Guelph, Guelph, Ontario, Canada
Linkang Zhang
Canadian Research Institute for Food Safety, Department of Food Science, University of Guelph, Guelph, Ontario, Canada
Valeria R. Parreira
Canadian Research Institute for Food Safety, Department of Food Science, University of Guelph, Guelph, Ontario, Canada
R. Stephen Brown
Department of Chemistry, Queen's University, Kingston, Ontario, Canada
Charles Chettleburgh
School of Environmental Sciences, University of Guelph, Guelph, Ontario, Canada
Nora Dannah
Department of Chemistry and Biology, Ryerson University, Toronto, Ontario, Canada
Robert Delatolla
Department of Civil Engineering, University of Ottawa, Ottawa, Ontario, Canada
Kimberly A. Gilbride
Department of Chemistry and Biology, Ryerson University, Toronto, Ontario, Canada
Urban Water Research Centre, Ryerson University, Toronto, Ontario, Canada
Tyson E. Graber
Children's Hospital of Eastern Ontario Research Institute, Ottawa, Ontario, Canada
Golam Islam
Faculty of Science, Ontario Tech University, Oshawa, Ontario, Canada
James Knockleby
Health Sciences North Research Institute, Sudbury, Ontario, Canada
Sean Ma
School of Environmental Sciences, University of Guelph, Guelph, Ontario, Canada
Hanlan McDougall
School of Environmental Sciences, University of Guelph, Guelph, Ontario, Canada
Great Lakes Institute for Environmental Research, University of Windsor, Windsor, Ontario, Canada
Aleksandra Mloszewska
Health Sciences North Research Institute, Sudbury, Ontario, Canada
Claire Oswald
Urban Water Research Centre, Ryerson University, Toronto, Ontario, Canada
Department of Geography and Environmental Studies, Ryerson University, Toronto, Ontario, Canada
Mark Servos
Department of Biology, University of Waterloo, Waterloo, Ontario, Canada
Megan Swinwood-Sky
School of Environmental Sciences, University of Guelph, Guelph, Ontario, Canada
Gustavo Ybazeta
Health Sciences North Research Institute, Sudbury, Ontario, Canada
Marc Habash
School of Environmental Sciences, University of Guelph, Guelph, Ontario, Canada
Lawrence Goodridge [email protected]
Canadian Research Institute for Food Safety, Department of Food Science, University of Guelph, Guelph, Ontario, Canada

Editor

Simon Roux
Editor
DOE Joint Genome Institute

Notes

Opeyemi U. Lawal, Linkang Zhang, and Valeria R. Parreira contributed equally to this article. The order of names of co-first author was unanimously determined among the authors.
The authors declare no conflict of interest.

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